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The Quartet does not play alone
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ScienceDirect Physics of Life Reviews 13 (2015) 71–72 www.elsevier.com/locate/plrev
Comment
The Quartet does not play alone Comment on “The quartet theory of human emotions: An integrative and neurofunctional model” by S. Koelsch et al. Josep Marco-Pallarés a,b,∗ , Ernest Mas-Herrero b a Department of Basic Psychology, Faculty of Psychology, University of Barcelona, Spain b Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, IDIBELL, L’Hospitalet de Llobregat, Barcelona, Spain
Received 14 April 2015; accepted 15 April 2015 Available online 16 April 2015 Communicated by L. Perlovsky
The study of emotions has been an important topic in cognitive and affective neuroscience in the last decades. In the present manuscript, Koelsch et al. [1] propose a new neurobiological framework based on four emotional core systems (the Quartet), involved in different aspects of human emotion processing. This is an interesting theory that goes beyond classical emotion classification to describe the emotional experience based on four main cerebral components (brainstem, diencephalon, hippocampus, and orbitofrontal cortex). This approach allows the description of different classes of affects, including those that are unique in humans as emotional responses associated to abstract stimuli (for example, aesthetical stimuli such as art and music). The theory extensively addresses the role of the different components of the Quartet in emotion processing, but it lacks of a proper integration with other fundamental systems, which play a critical role in the emotion experience. In concrete, an important aspect in emotion processing is the interaction between sensory and perceptual systems and the different core components of the emotional network. Indeed, although the relevance of these interactions is often underrepresented in the literature, the emotional experience does not only depend on the functioning of a few cerebral regions, but on a more extensive functional network, which implies, among others, the processing of sensory information. Indeed, humans can experience an enormous diversity of emotions from a broad range of stimuli. For example, in the auditory domain, emotions can be elicited either by basic sounds, such as the cry of a baby, or by very complex acoustic stimuli, such as a Mahler’s symphony. Independently of the source and the complexity, all emotional stimuli might engage the four components proposed in the present framework. However, one might be more prone to emotionally react to certain stimulus than to others although all of them engage the same emotional network. In addition, different people might react very differently to a certain type of emotional stimulus (e.g., music), while presenting similar emotional response to another one (e.g., money) [2,3]. One potential mechanism to explain such large inter- and intra-individual differences is the interaction between the brain areas of the core emotional system and those involved in sensation and perception. Therefore, understanding how the sensory information reaches the different components of the Quartet might be a crucial aspect to provide an integrative theory of emotion processing. DOI of original article: http://dx.doi.org/10.1016/j.plrev.2015.03.001. * Corresponding author.
E-mail address: [email protected] (J. Marco-Pallarés). http://dx.doi.org/10.1016/j.plrev.2015.04.015 1571-0645/© 2015 Elsevier B.V. All rights reserved.
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J. Marco-Pallarés, E. Mas-Herrero / Physics of Life Reviews 13 (2015) 71–72
The only reference of the proposed theory to the processing of sensory information is the role of the Orbitofrontal Cortex in emotional appraisal through Stimulus Evaluation Checks [4]. However, the interaction between sensory information and the core areas of emotion processing is far more complex. The different components of the Quartet receive sensory information with different degrees of processing. For example, direct inputs from most of the sensory modalities are sent to the diencephalon (and specifically the thalamus) which, in turn, relies this information to the cortex. This information, with different levels of processing, is then sent to the OFC [5], and to the hippocampus through the entorhinal cortex [6]. The strength of these sensory-emotion interactions could provide an alternative biological explanation for the described emotion processing differences between and within individuals, rather than the inner functioning of the emotional system. For instance, studies of musical emotion have shown that music-induced emotion could be driven in part by the interaction between the ventral striatum and the auditory cortex [7]. In line with these results, Koelsch et al. [8] showed that the interaction between auditory cortex and amygdala plays an important role in music-evoked fear and joy. These two results highlight the relevance of auditory cortex in the experience of music emotion beyond classical limbic and cortical structures involved in emotional processing. Further, a recent study has also identified a group of healthy people who do not emotionally react to music but, in contrast, present standard emotional reaction to other types of rewards (specific music anhedonia [2,9]). This finding suggests that the selective engagement of the emotional circuits critically depends on the characteristic of the stimulus. In addition, lesion studies have also provided important insights in this topic. Within the last two decades, three case studies have been published reporting individuals that lost the capacity of feeling emotions from music after brain damage in different regions (temporal and parietal cortices, insula and amygdala), none of them being part of the Quartet [10–12]. Thus, although the Quartet might represent the ultimate stage of a hierarchical emotional processing, brain regions involved in sensory and perceptual integration might act as portal for the entrance of sensory information into the emotional system. Probably the Quartet is playing the main section in emotion processing, but it is not playing alone. Acknowledgement J.M.P. acknowledges support from the Spanish Government grant PSI2012-37472. References [1] Koelsch S, Jacobs AM, Menninghaus W, Liebal K, Klann-Delius G, von Scheve G, et al. The quartet theory of human emotions: an integrative and neurofunctional model. Phys Life Rev 2015;13:1–27 [in this issue]. [2] Mas-Herrero E, Zatorre RJ, Rodriguez-Fornells A, Marco-Pallarés J. Dissociation between musical and monetary reward responses in specific musical anhedonia. Curr Biol 2014;24:699–704. [3] Sescousse G, Barbalat G, Domenech P, Dreher JC. Imbalance in the sensitivity to different types of rewards in pathological gambling. Brain 2013;136:2527–38. [4] Schere KR. Appraisal considered as a process of multilevel sequential checking. In: Scherer KR, Schorr A, Johnstone T, editors. Appraisal processes in emotion: theory, methods, research. NY: Oxford University Press; 2001. p. 120–44. [5] Haber SN. Neuroanatomy of reward: a view from the Ventral Striatum. In: Gottfried JA, editor. Neurobiology of sensation and reward. Boca Raton (FL): CRC Press; 2011. [6] Canning KJ, Leung LS. Lateral entorhinal, perirhinal, and amygdala-entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: a current source density study. Hippocampus 1997;7:643–55. [7] Salimpoor VN, van den Bosch I, Kovacevic N, McIntosh AR, Dagher A, Zatorre RJ. Interactions between the nucleus accumbens and auditory cortices predict music reward value. Science 2013;340:216–9. [8] Koelsch S, Skouras S, Fritz T, Herrera P, Bonhage C, Kussner MB, et al. The roles of superficial amygdala and auditory cortex in music-evoked fear and joy. NeuroImage 2013;81:49–60. [9] Mas-Herrero E, Marco-Pallares J, Lorenzo-Seva U, Zatorre RJ, Rodriguez-Fornells A. Individual differences in music reward experiences. Music Percept 2013;31:118–38. [10] Mazzoni M, Moretti P, Pardossi L, Vista M, Muratorio A, Puglioli M. A case of music imperceptions. J Neurol Neurosurg Psychiatry 1993;56:322. [11] Griffiths TD, Warren TD, Dean JL, Howard D. “When the feeling’s gone”: a selective loss of musical emotion. J Neurol Neurosurg Psychiatry 2004;75:344–5. [12] Satoh M, Nakase T, Nagata K, Tomimoto H. Musical anhedonia: selective loss of emotional experience in listening to music. Neurocase 2011;17:410–7.
ScienceDirect Physics of Life Reviews 13 (2015) 71–72 www.elsevier.com/locate/plrev
Comment
The Quartet does not play alone Comment on “The quartet theory of human emotions: An integrative and neurofunctional model” by S. Koelsch et al. Josep Marco-Pallarés a,b,∗ , Ernest Mas-Herrero b a Department of Basic Psychology, Faculty of Psychology, University of Barcelona, Spain b Cognition and Brain Plasticity Group, Bellvitge Biomedical Research Institute, IDIBELL, L’Hospitalet de Llobregat, Barcelona, Spain
Received 14 April 2015; accepted 15 April 2015 Available online 16 April 2015 Communicated by L. Perlovsky
The study of emotions has been an important topic in cognitive and affective neuroscience in the last decades. In the present manuscript, Koelsch et al. [1] propose a new neurobiological framework based on four emotional core systems (the Quartet), involved in different aspects of human emotion processing. This is an interesting theory that goes beyond classical emotion classification to describe the emotional experience based on four main cerebral components (brainstem, diencephalon, hippocampus, and orbitofrontal cortex). This approach allows the description of different classes of affects, including those that are unique in humans as emotional responses associated to abstract stimuli (for example, aesthetical stimuli such as art and music). The theory extensively addresses the role of the different components of the Quartet in emotion processing, but it lacks of a proper integration with other fundamental systems, which play a critical role in the emotion experience. In concrete, an important aspect in emotion processing is the interaction between sensory and perceptual systems and the different core components of the emotional network. Indeed, although the relevance of these interactions is often underrepresented in the literature, the emotional experience does not only depend on the functioning of a few cerebral regions, but on a more extensive functional network, which implies, among others, the processing of sensory information. Indeed, humans can experience an enormous diversity of emotions from a broad range of stimuli. For example, in the auditory domain, emotions can be elicited either by basic sounds, such as the cry of a baby, or by very complex acoustic stimuli, such as a Mahler’s symphony. Independently of the source and the complexity, all emotional stimuli might engage the four components proposed in the present framework. However, one might be more prone to emotionally react to certain stimulus than to others although all of them engage the same emotional network. In addition, different people might react very differently to a certain type of emotional stimulus (e.g., music), while presenting similar emotional response to another one (e.g., money) [2,3]. One potential mechanism to explain such large inter- and intra-individual differences is the interaction between the brain areas of the core emotional system and those involved in sensation and perception. Therefore, understanding how the sensory information reaches the different components of the Quartet might be a crucial aspect to provide an integrative theory of emotion processing. DOI of original article: http://dx.doi.org/10.1016/j.plrev.2015.03.001. * Corresponding author.
E-mail address: [email protected] (J. Marco-Pallarés). http://dx.doi.org/10.1016/j.plrev.2015.04.015 1571-0645/© 2015 Elsevier B.V. All rights reserved.
72
J. Marco-Pallarés, E. Mas-Herrero / Physics of Life Reviews 13 (2015) 71–72
The only reference of the proposed theory to the processing of sensory information is the role of the Orbitofrontal Cortex in emotional appraisal through Stimulus Evaluation Checks [4]. However, the interaction between sensory information and the core areas of emotion processing is far more complex. The different components of the Quartet receive sensory information with different degrees of processing. For example, direct inputs from most of the sensory modalities are sent to the diencephalon (and specifically the thalamus) which, in turn, relies this information to the cortex. This information, with different levels of processing, is then sent to the OFC [5], and to the hippocampus through the entorhinal cortex [6]. The strength of these sensory-emotion interactions could provide an alternative biological explanation for the described emotion processing differences between and within individuals, rather than the inner functioning of the emotional system. For instance, studies of musical emotion have shown that music-induced emotion could be driven in part by the interaction between the ventral striatum and the auditory cortex [7]. In line with these results, Koelsch et al. [8] showed that the interaction between auditory cortex and amygdala plays an important role in music-evoked fear and joy. These two results highlight the relevance of auditory cortex in the experience of music emotion beyond classical limbic and cortical structures involved in emotional processing. Further, a recent study has also identified a group of healthy people who do not emotionally react to music but, in contrast, present standard emotional reaction to other types of rewards (specific music anhedonia [2,9]). This finding suggests that the selective engagement of the emotional circuits critically depends on the characteristic of the stimulus. In addition, lesion studies have also provided important insights in this topic. Within the last two decades, three case studies have been published reporting individuals that lost the capacity of feeling emotions from music after brain damage in different regions (temporal and parietal cortices, insula and amygdala), none of them being part of the Quartet [10–12]. Thus, although the Quartet might represent the ultimate stage of a hierarchical emotional processing, brain regions involved in sensory and perceptual integration might act as portal for the entrance of sensory information into the emotional system. Probably the Quartet is playing the main section in emotion processing, but it is not playing alone. Acknowledgement J.M.P. acknowledges support from the Spanish Government grant PSI2012-37472. References [1] Koelsch S, Jacobs AM, Menninghaus W, Liebal K, Klann-Delius G, von Scheve G, et al. The quartet theory of human emotions: an integrative and neurofunctional model. Phys Life Rev 2015;13:1–27 [in this issue]. [2] Mas-Herrero E, Zatorre RJ, Rodriguez-Fornells A, Marco-Pallarés J. Dissociation between musical and monetary reward responses in specific musical anhedonia. Curr Biol 2014;24:699–704. [3] Sescousse G, Barbalat G, Domenech P, Dreher JC. Imbalance in the sensitivity to different types of rewards in pathological gambling. Brain 2013;136:2527–38. [4] Schere KR. Appraisal considered as a process of multilevel sequential checking. In: Scherer KR, Schorr A, Johnstone T, editors. Appraisal processes in emotion: theory, methods, research. NY: Oxford University Press; 2001. p. 120–44. [5] Haber SN. Neuroanatomy of reward: a view from the Ventral Striatum. In: Gottfried JA, editor. Neurobiology of sensation and reward. Boca Raton (FL): CRC Press; 2011. [6] Canning KJ, Leung LS. Lateral entorhinal, perirhinal, and amygdala-entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: a current source density study. Hippocampus 1997;7:643–55. [7] Salimpoor VN, van den Bosch I, Kovacevic N, McIntosh AR, Dagher A, Zatorre RJ. Interactions between the nucleus accumbens and auditory cortices predict music reward value. Science 2013;340:216–9. [8] Koelsch S, Skouras S, Fritz T, Herrera P, Bonhage C, Kussner MB, et al. The roles of superficial amygdala and auditory cortex in music-evoked fear and joy. NeuroImage 2013;81:49–60. [9] Mas-Herrero E, Marco-Pallares J, Lorenzo-Seva U, Zatorre RJ, Rodriguez-Fornells A. Individual differences in music reward experiences. Music Percept 2013;31:118–38. [10] Mazzoni M, Moretti P, Pardossi L, Vista M, Muratorio A, Puglioli M. A case of music imperceptions. J Neurol Neurosurg Psychiatry 1993;56:322. [11] Griffiths TD, Warren TD, Dean JL, Howard D. “When the feeling’s gone”: a selective loss of musical emotion. J Neurol Neurosurg Psychiatry 2004;75:344–5. [12] Satoh M, Nakase T, Nagata K, Tomimoto H. Musical anhedonia: selective loss of emotional experience in listening to music. Neurocase 2011;17:410–7.